Role of inflammatory infiltrates in triple negative breast cancer

Journal of Clinical Pathology

Volumn 68, Issue 7, 2015, Pages 506-510

  Matsumoto, Hirofumi ^a,b   Koo, Si Lin ^c   Dent, Rebecca ^c   Tan, Puay Hoon ^a   Iqbal, Jabed ^a  

^a SINGAPORE GENERAL HOSPITAL   (Singapore)

^b UNIVERSITY HOSPITAL OF THE RYUKYUS   (Japan)

^c DIVISION OF MEDICAL ONCOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

DIFFERENTIATION ANTIGEN; INTERLEUKIN 6; NY ESO 1 ANTIGEN; PROTEIN P53; VIRUS ANTIGEN; TUMOR MARKER;

ARTICLE; CANCER CHEMOTHERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; DENDRITIC CELL; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOSUPPRESSIVE TREATMENT; MACROPHAGE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; TRIPLE NEGATIVE BREAST CANCER; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT; ANIMAL; CHEMISTRY; FEMALE; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; INFLAMMATION; PATHOLOGY; PHENOTYPE; PROCEDURES; PROGNOSIS; TRIPLE NEGATIVE BREAST NEOPLASMS;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; IMMUNOTHERAPY; INFLAMMATION; LYMPHOCYTES, TUMOR-INFILTRATING; MACROPHAGES; PHENOTYPE; PROGNOSIS; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR MARKERS, BIOLOGICAL; TUMOR MICROENVIRONMENT;

EID: 84933181457     PISSN: 00219746     EISSN: 14724146     Source Type: Journal    
DOI: 10.1136/jclinpath-2015-202944     Document Type: Article

References (78)

1. Reis-Filho JS, Tutt ANJ. Triple negative tumours: a critical review. Histopathology 2008;52:108-18.
2. Criscitiello C, Azim HA, Schouten PC, et al. Understanding the biology of triple-negative breast cancer. Ann Oncol 2012;23(Suppl 6):vi13-18.
3. Lehmann BD, Bauer JA, Chen X, et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 2011;121:2750-67.
4. Stagg J, Allard B. Immunotherapeutic approaches in triple-negative breast cancer: latest research and clinical prospects. Ther Adv Med Oncol 2013;5:169-81.
5. Ioachim HL, Dorsett BH, Paluch E. The immune response at the tumor site in lung carcinoma. Cancer 1976;38:2296-309.
6. Moore OS, Foote FW. The relatively favorable prognosis of medullary carcinoma of the breast. Cancer 1949;2:635-42.
7. Yu P, Fu YX. Tumor-infiltrating T lymphocytes: friends or foes? Lab Invest 2006;86:231-45.
8. Naito Y, Saito K, Shiiba K, et al. CD8+ T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer. Cancer Res 1998;58:3491-4.
9. Schumacher K, Haensch W, Röefzaad C, et al. Prognostic significance of activated CD8(+) T cell infiltrations within esophageal carcinomas. Cancer Res 2001;61:3932-6.
10. Fukunaga A, Miyamoto M, Cho Y, et al. CD8+ tumor-infiltrating lymphocytes together with CD4+ tumor-infiltrating lymphocytes and dendritic cells improve the prognosis of patients with pancreatic adenocarcinoma. Pancreas 2004;28:e26-31.
11. Hiraoka K, Miyamoto M, Cho Y, et al. Concurrent infiltration by CD8+ T cells and CD4+ T cells is a favourable prognostic factor in non-small-cell lung carcinoma. Br J Cancer 2006;94:275-80.
12. Al-Shibli KI, Donnem T, Al-Saad S, et al. Prognostic effect of epithelial and stromal lymphocyte infiltration in non-small cell lung cancer. Clin Cancer Res 2008;14:5220-7.
13. Tanchot C, Terme M, Pere H, et al. Tumor-infiltrating regulatory T cells: phenotype, role, mechanism of expansion in situ and clinical significance. Cancer Microenviron 2013;6:147-57.
14. Curiel TJ, Coukos G, Zou L, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004;10:942-9.
15. Bron L, Jandus C, Andrejevic-Blant S, et al. Prognostic value of arginase-II expression and regulatory T-cell infiltration in head and neck squamous cell carcinoma. Int J Cancer 2013;132:E85-93.
16. Winerdal ME, Marits P, Winerdal M, et al. FOXP3 and survival in urinary bladder cancer. BJU Int 2011;108:1672-8.
17. Allavena P, Mantovani A. Immunology in the clinic review series; focus on cancer: tumour-associated macrophages: undisputed stars of the inflammatory tumour microenvironment. Clin Exp Immunol 2012;167:195-205.
18. Bingle L, Brown NJ, Lewis CE. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol 2002;196:254-65.
19. Mahmoud SMA, Paish EC, Powe DG, et al. Tumor-infiltrating CD8+ lymphocytes predict clinical outcome in breast cancer. J Clin Oncol 2011;29:1949-5
20. Liu S, Lachapelle J, Leung S, et al. CD8+ lymphocyte infiltration is an independent favorable prognostic indicator in basal-like breast cancer. Breast Cancer Res 2012;14:R48.
21. Baker K, Lachapelle J, Zlobec I, et al. Prognostic significance of CD8+ T lymphocytes in breast cancer depends upon both oestrogen receptor status and histological grade. Histopathology 2011;58:1107-16.
22. Teschendorff AE, Miremadi A, Pinder SE, et al. An immune response gene expression module identifies a good prognosis subtype in estrogen receptor negative breast cancer. Genome Biol 2007;8:R157.
23. Teschendorff AE, Gomez S, Arenas A, et al. Improved prognostic classification of breast cancer defined by antagonistic activation patterns of immune response pathway modules. BMC Cancer 2010;10:604.
24. Bohling SD, Allison KH. Immunosuppressive regulatory T cells are associated with aggressive breast cancer phenotypes: a potential therapeutic target. Mod Pathol 2008;21:1527-32.
25. Mahmoud SMA, Paish EC, Powe DG, et al. An evaluation of the clinical significance of FOXP3+ infiltrating cells in human breast cancer. Breast Cancer Res Treat 2011;127:99-108.
26. Droeser R, Zlobec I, Kilic E, et al. Differential pattern and prognostic significance of CD4+, FOXP3+ and IL-17+ tumor infiltrating lymphocytes in ductal and lobular breast cancers. BMC Cancer 2012;12:134.
27. Bates GJ, Fox SB, Han C, et al. Quantification of regulatory T cells enables the identification of high-risk breast cancer patients and those at risk of late relapse. J Clin Oncol 2006;24:5373-80.
28. West NR, Kost SE, Martin SD, et al. Tumour-infiltrating FOXP3(+) lymphocytes are associated with cytotoxic immune responses and good clinical outcome in oestrogen receptor-negative breast cancer. Br J Cancer 2013;108:155-62.
29. Lee S, Cho EY, Park YH, et al. Prognostic impact of FOXP3 expression in triple-negative breast cancer. Acta Oncol 2013;52:73-81.
30. Leek RD, Lewis CE, Whitehouse R, et al. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res 1996;56:4625-9.
31. Mahmoud SMA, Lee AHS, Paish EC, et al. Tumour-infiltrating macrophages and clinical outcome in breast cancer. J Clin Pathol 2012;65:159-63.
32. Medrek C, Pontén F, Jirström K, et al. The presence of tumor associated macrophages in tumor stroma as a prognostic marker for breast cancer patients. BMC Cancer 2012;12:306.
33. Stewart DA, Yang Y, Makowski L, et al. Basal-like breast cancer cells induce phenotypic and genomic changes in macrophages. Mol Cancer Res 2012;10:727-38.
34. Schulz DM, Böllner C, Thomas G, et al. Identification of differentially expressed proteins in triple-negative breast carcinomas using DIGE and mass spectrometry. J Proteome Res 2009;8:3430-8.
35. Ha NH, Nair VS, Reddy DNS, et al. Lactoferrin-endothelin-1 axis contributes to the development and invasiveness of triple-negative breast cancer phenotypes. Cancer Res 2011;71:7259-69.
36. Wolf JS, Li G, Varadhachary A, et al. Oral lactoferrin results in T cell-dependent tumor inhibition of head and neck squamous cell carcinoma in vivo. Clin Cancer Res 2007;13:1601-10.
37. Yang D, de la Rosa G, Tewary P, et al. Alarmins link neutrophils and dendritic cells. Trends Immunol 2009;30:531-7.
38. Roxanis I. Occurrence and significance of epithelial-mesenchymal transition in breast cancer. J Clin Pathol 2013;66:517-21.
39. Al-Hajj M, Wicha MS, Benito-Hernandez A, et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003;100:3983-8.
40. Reiman JM, Knutson KL, Radisky DC. Immune promotion of epithelial-mesenchymal transition and generation of breast cancer stem cells. Cancer Res 2010;70:3005-8.
41. Sarrió D, Rodriguez-Pinilla SM, Hardisson D, et al. Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res 2008;68:989-97.
42. Honeth G, Bendahl PO, Ringnér M, et al. The CD44+/CD24- phenotype is enriched in basal-like breast tumors. Breast Cancer Res 2008;10:R53.
43. Denkert C, Loibl S, Noske A, et al. Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol 2010;28:105-13.
44. Yamaguchi R, Tanaka M, Yano A, et al. Tumor-infiltrating lymphocytes are important pathologic predictors for neoadjuvant chemotherapy in patients with breast cancer. Hum Pathol 2012;43:1688-94.
45. Lee HJ, Seo JY, Ahn JH, et al. Tumor-associated lymphocytes predict response to neoadjuvant chemotherapy in breast cancer patients. J Breast Cancer 2013;16:32-9.
46. Seo AN, Lee HJ, Kim EJ, et al. Tumour-infiltrating CD8+ lymphocytes as an independent predictive factor for pathological complete response to primary systemic therapy in breast cancer. Br J Cancer 2013;109:2705-13.
47. West NR, Milne K, Truong PT, et al. Tumor-infiltrating lymphocytes predict response to anthracycline-based chemotherapy in estrogen receptor-negative breast cancer. Breast Cancer Res 2011;13:R126.
48. Ono M, Tsuda H, Shimizu C, et al. Tumor-infiltrating lymphocytes are correlated with response to neoadjuvant chemotherapy in triple-negative breast cancer. Breast Cancer Res Treat 2012;132:793-805.
49. Demaria S, Volm MD, Shapiro RL, et al. Development of tumor-infiltrating lymphocytes in breast cancer after neoadjuvant paclitaxel chemotherapy. Clin Cancer Res 2001;7:3025-30.
50. Apetoh L, Ghiringhelli F, Tesniere A, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007;13:1050-9.
51. Ladoire S, Arnould L, Apetoh L, et al. Pathologic complete response to neoadjuvant chemotherapy of breast carcinoma is associated with the disappearance of tumor-infiltrating foxp3+ regulatory T cells. Clin Cancer Res 2008;14:2413-20.
52. van der Most RG, Currie AJ, Cleaver AL, et al. Cyclophosphamide chemotherapy sensitizes tumor cells to TRAIL-dependent CD8 T cell-mediated immune attack resulting in suppression of tumor growth. PLoS ONE 2009;4:e6982.
53. Chen YT, Ross DS, Chiu R, et al. Multiple cancer/testis antigens are preferentially expressed in hormone-receptor negative and high-grade breast cancers. PLoS ONE 2011;6:e17876.
54. Grigoriadis A, Caballero OL, Hoek KS, et al. CT-X antigen expression in human breast cancer. Proc Natl Acad Sci U S A 2009;106:13493-8.
55. Curigliano G, Viale G, Ghioni M, et al. Cancer-testis antigen expression in triple-negative breast cancer. Ann Oncol 2011;22:98-103.
56. Ademuyiwa FO, Bshara W, Attwood K, et al. NY-ESO-1 cancer testis antigen demonstrates high immunogenicity in triple negative breast cancer. PLoS ONE 2012;7:e38783.
57. Karn T, Pusztai L, Ruckhäberle E, et al. Melanoma antigen family A identified by the bimodality index defines a subset of triple negative breast cancers as candidates for immune response augmentation. Eur J Cancer 2012;48:12-23.
58. Scandiuzzi L, Ghosh K, Zang X. T cell costimulation and coinhibition: genetics and disease. Discov Med 2011;12:119-28.
59. Ghebeh H, Mohammed S, Al-Omair A, et al. The B7-H1 (PD-L1) T lymphocyte-inhibitory molecule is expressed in breast cancer patients with infiltrating ductal carcinoma: correlation with important high-risk prognostic factors. Neoplasia 2006;8:190-8.
60. Ghebeh H, Tulbah A, Mohammed S, et al. Expression of B7-H1 in breast cancer patients is strongly associated with high proliferative Ki-67-expressing tumor cells. Int J Cancer 2007;121:751-8.
61. Soliman H, Khalil F, Antonia S. PD-L1 expression is increased in a subset of basal type breast cancer cells. PLoS ONE 2014;9:e88557.
62. Topalian SL, Drake CG, Pardoll DM. Targeting the PD-1/B7-H1(PD-L1) pathway to activate anti-tumor immunity. Curr Opin Immunol 2012;24:207-12.
63. Mittendorf EA, Philips AV, Meric-Bernstam F, et al. PD-L1 expression in triple-negative breast cancer. Cancer Immunol Res 2014;2:361-70.
64. Lespagnard L, Gancberg D, Rouas G, et al. Tumor-infiltrating dendritic cells in adenocarcinomas of the breast: a study of 143 neoplasms with a correlation to usual prognostic factors and to clinical outcome. Int J Cancer 1999;84:309-14.
65. Iwamoto M, Shinohara H, Miyamoto A, et al. Prognostic value of tumor-infiltrating dendritic cells expressing CD83 in human breast carcinomas. Int J Cancer 2003;104:92-7.
66. Coventry BJ, Morton J. CD1a-positive infiltrating-dendritic cell density and 5-year survival from human breast cancer. Br J Cancer 2003;89:533-8.
67. Sisirak V, Faget J, Gobert M, et al. Impaired IFN-α production by plasmacytoid dendritic cells favors regulatory T-cell expansion that may contribute to breast cancer progression. Cancer Res 2012;72:5188-97.
68. Chavey C, Bibeau F, Gourgou-Bourgade S, et al. Oestrogen receptor negative breast cancers exhibit high cytokine content. Breast Cancer Res 2007;9:R15.
69. Deng XS, Wang S, Deng A, et al. Metformin targets Stat3 to inhibit cell growth and induce apoptosis in triple-negative breast cancers. Cell Cycle 2012;11:367-76.
70. Hartman ZC, Poage GM, den Hollander P, et al. Growth of triple-negative breast cancer cells relies upon coordinate autocrine expression of the proinflammatory cytokines IL-6 and IL-8. Cancer Res 2013;73:3470-80.
71. van 't Veer LJ, Dai H, van de Vijver MJ, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002;415:530-6.
72. Rody A, Karn T, Liedtke C, et al. A clinically relevant gene signature in triple negative and basal-like breast cancer. Breast Cancer Res 2011;13:R97.
73. Arranz EE, Vara JÁF, Gámez-Pozo A, et al. Gene signatures in breast cancer: current and future uses. Transl Oncol 2012;5:398-403.
74. Hanker LC, Rody A, Holtrich U, et al. Prognostic evaluation of the B cell/IL-8 metagene in different intrinsic breast cancer subtypes. Breast Cancer Res Treat 2013;137:407-16.
75. Yau C, Esserman L, Moore DH, et al. A multigene predictor of metastatic outcome in early stage hormone receptor-negative and triple-negative breast cancer. Breast Cancer Res 2010;12:R85.
76. Chen X, Iliopoulos D, Zhang Q, et al. XBP1 promotes triple-negative breast cancer by controlling the HIF1a pathway. Nature 2014;508:103-7.
77. Montagner M, Enzo E, Forcato M, et al. SHARP1 suppresses breast cancer metastasis by promoting degradation of hypoxia-inducible factors. Nature 2012;487:380-4.
78. Palazón A, Aragonés J, Morales-Kastresana A, et al. Molecular pathways: hypoxia response in immune cells fighting or promoting cancer. Clin Cancer Res 2012;18:1207-13.